Functional connectivity-based attractor dynamics of the human brain in rest, task, and disease.

Abstract

Functional brain connectivity has been instrumental in uncovering the large-scale organization of the brain and its relation to various behavioral and clinical phenotypes. Understanding how this functional architecture relates to the brain's dynamic activity repertoire is an essential next step towards interpretable generative models of brain function. We propose functional connectivity-based Attractor Neural Networks (fcANNs), a theoretically inspired model of macro-scale brain dynamics, simulating recurrent activity flow among brain regions based on first principles of self-organization. In the fcANN framework, brain dynamics are understood in relation to attractor states; neurobiologically meaningful activity configurations that minimize the free energy of the system. We provide the first evidence that large-scale brain attractors - as reconstructed by fcANNs - exhibit an approximately orthogonal organization, which is a signature of the self-orthogonalization mechanism of the underlying theoretical framework of free-energy-minimizing attractor networks. Analyses of seven distinct human neuroimaging datasets demonstrate that fcANNs can accurately reconstruct and predict brain dynamics under a wide range of conditions, including resting and task states, and brain disorders. By establishing a formal link between connectivity and activity, fcANNs offer a simple and interpretable computational alternative to conventional descriptive analyses.